Talking to Cows: Reactions to Different Auditory Stimuli During Gentle Human-Animal Interactions

Talking to Cows: Reactions to Different Auditory Stimuli During Gentle Human-Animal Interactions. Annika Lange et al. Front. Psychol., October 15 2020. https://doi.org/10.3389/fpsyg.2020.579346

Abstract: The quality of the animal-human relationship and, consequently, the welfare of animals can be improved by gentle interactions such as stroking and talking. The perception of different stimuli during these interactions likely plays a key role in their emotional experience, but studies are scarce. During experiments, the standardization of verbal stimuli could be increased by using a recording. However, the use of a playback might influence the perception differently than “live” talking, which is closer to on-farm practice. Thus, we compared heifers' (n = 28) reactions to stroking while an experimenter was talking soothingly (“live”) or while a recording of the experimenter talking soothingly was played (“playback”). Each animal was tested three times per condition and each trial comprised three phases: pre-stimulus, stimulus (stroking and talking) and post-stimulus. In both conditions, similar phrases with positive content were spoken calmly, using long low-pitched vowels. All tests were video recorded and analyzed for behaviors associated with different affective states. Effects on the heifers' cardiac parameters were assessed using analysis of heart rate variability. Independently of the auditory stimuli, longer durations of neck stretching occurred during stroking, supporting our hypothesis of a positive perception of stroking. Observation of ear positions revealed longer durations of the “back up” position and less ear flicking and changes of ear positions during stroking. The predicted decrease in HR during stroking was not confirmed; instead we found a slightly increased mean HR during stroking with a subsequent decrease in HR, which was stronger after stroking with live talking. In combination with differences in HRV parameters, our findings suggest that live talking might have been more pleasurable to the animals and had a stronger relaxing effect than “playback.” The results regarding the effects of the degree of standardization of the stimulus on the variability of the data were inconclusive. We thus conclude that the use of recorded auditory stimuli to promote positive affective states during human-animal interactions in experimental settings is possible, but not necessarily preferable.

Discussion

We compared the reactions of heifers to stroking while applying two different auditory stimuli: the stroker talking directly to the animals in a gentle voice or a recording of the stroker's talking. We found behavioral and physiological indications of a positive perception of the interactions for both auditory stimuli. While the behavioral reactions to gentle interactions did not differ statistically, some of the cardiac parameters indicated differences between the auditory stimuli, also shortly after the presentation of the stimulus had ended.

Perception of Each Treatment

Both treatments led to changes in behavior during the STIM phase that indicate a positive perception: During stroking, the heifers showed significantly longer durations of neck stretching, a behavior shown during intraspecific social grooming (Sambraus, 1969; Reinhardt et al., 1986; Schmied et al., 2005), which is often actively solicited, and stroking by humans (Waiblinger et al., 2004; Schmied et al., 2008; Lürzel et al., 2015a). It is interpreted a sign of enjoyment, and it can thus be assumed that the situation is perceived as positive.

In a previous, similar experiment (Lange et al., 2020), we observed decreases of ear flicking and changes of ear position during stroking with no auditory stimuli. The present study confirms this pattern. The animals showed less ear flicking during STIM than PRE, a behavior mostly associated with negative affective states, such as pain after dehorning (Heinrich et al., 2010; Neave et al., 2013) or reactions to insect attacks (Mooring et al., 2007).

During STIM, the animals also changed the positions of their ears less often than in PRE. Frequencies of changes of ear positions were lower in sheep feeding (Reefmann et al., 2009a) or voluntarily being groomed by a human (Reefmann et al., 2009b) than during separation from the herd. In contrast, dairy cows showed an increased frequency of changes of ear positions during stroking compared to before or after (Proctor and Carder, 2014), which might however have been caused by small differences in experimental design, such as the stroker approaching at the beginning of the stroking phase. In contrast, the decrease in changes of ear positions and ear flicking during stroking in the current as well as in our previous study (Lange et al., 2020) indicates an association of a reduction of these behaviors with a positive, low-arousal state also in cattle.

However, for some of the behaviors we expected to indicate affective states, the treatment did not lead to significant differences: previously observed effects of stroking (Lange et al., 2020) on the duration of the animal resting its head and the time spent in contact with the experimenter were not confirmed in this study. These findings might be connected with the auditory stimulus, which might keep the animal comparatively more attentive to a certain degree and thus limit the intensity of the relaxation.

In an attempt to reflect the continuous nature of ear positions, we recorded nine different positions along the vertical and the horizontal axis: back up, back center, back down, center up, center, center down, forward up, forward center and forward down, plus ear hanging. During stroking, durations of the back up position increased significantly, while durations of forward up and ear low decreased, mostly in line with our previous experiment (Lange et al., 2020). The tendency toward decreased durations of forward up might indicate lowered vigilance (Boissy and Dumont, 2002), which is associated with less fear (Welp et al., 2004), and could corroborate the hypothesis that stroking induces positive low-arousal states.

We predicted to find longer durations of ear low during stroking, because low ear positions, including ear hanging, were associated with low-arousal, positive affective states in dairy cows in previous studies (Schmied et al., 2008; Proctor and Carder, 2014). However, we observed predominantly back up positions and surprisingly rare occurrences of ear low. One possible reason might have been the strokers' position kneeling next to the lying animal and resulting in the auditory signal being located above and behind the heifers' ears in both conditions. Since the ear position pattern was very similar to the one found in our previous study without vocal stimulation (Lange et al., 2020), however, the effect of the auditory stimulus seems not to have had a strong influence on ear positions, possibly because cattle have a relatively low sound-localization acuity compared with other mammals (Heffner and Heffner, 1992); the stroker's position relative to the animal's head may nevertheless be relevant.

Furthermore, the effects that we saw in STIM were not observed in POST, contrary to our hypothesis of longer-lasting effects of the treatment on behavior. However, some of the observed behaviors (such as neck stretching and the different ear positions) are more immediate reactions to positive stimuli and do not allow to observe longer-lasting changes in affective states.

Comparison of the Treatments

As there were no significant differences in the behavioral reactions to the two different auditory stimuli, stroking and talking in a gentle voice per se seem to have a stronger effect on the behavior than the source of the auditory stimulus. As this experiment did not include a treatment where the animals were stroked without any auditory stimulation, we cannot infer any information on whether gentle talking in general enhances or diminishes the positive effects of stroking, but the results are very similar to our previous study, where the animals were stroked without acoustic stimulation. Stroking can elicit quite strong effects on physiology and behavior in different species (rats: Holst et al., 2005; cows: Schmied et al., 2010; cats: Gourkow et al., 2014; lambs: Coulon et al., 2015; horses: Lansade et al., 2018), which might exceed possible consequences of small differences in auditory stimuli. Regarding the absence of significant differences in behavior, it seems plausible that the heifers did not discern the two auditory stimuli, at least not to an extent where it would have affected their behavior. Furthermore, the mismatch of experimenter and playback voice did not have a significant effect on any of the behaviors. Indeed, there is a substantial amount of literature in different species indicating that they do not necessarily distinguish playback from live auditory stimuli: playback is used successfully in studies investigating bird behavior (Douglas and Mennill, 2010), dogs react to dog-directed human speech played back from a loudspeaker (Ben-Aderet et al., 2017; Benjamin and Slocombe, 2018), and dairy cows increase their production when exposed to a playback of calf vocalizations (Pollock and Hurnik, 1978; McCowan et al., 2002; no effect if calves are reared with their mothers: Zipp et al., 2013). Other characteristics of speech might thus have a stronger impact on the animals' behavior than the characteristics induced by the type of source.

On the other hand, the analysis of cardiac parameters points toward a different perception of the two auditory stimuli. In both conditions, HR increased from PRE to STIM and decreased from STIM to POST, but this decrease was significantly more pronounced in the “live” condition, indicating a stronger relaxation effect of live talking after the presentation of the stimulus. The slight increase of HR during STIM in both conditions seems to contradict our expectation that our treatment would induce a low-arousal state. However, it is in line with previous findings reporting an increased HR of lying animals that were licked by conspecifics (Laister et al., 2011) or receiving a stroking treatment (Lange et al., 2020) and might be caused by physical reactions to stroking (e.g., neck stretching) more than by a meaningful change in arousal or affective state (Lange et al., 2020).

Independently of the changes in HR, there were some significant effects of the conditions on HRV parameters: HF increased in POST in the “live” condition, but decreased in POST in the “playback” condition. It is widely accepted that HF increases with increasing activity of the parasympathetic branch of the autonomic nervous system (Task Force of ESP and NASPE, 1996; von Borell et al., 2007). The increased values suggest a higher parasympathetic activity after stroking in the “live,” but not the “playback” condition. An increased HF may be associated with positive emotions (McCraty et al., 1995; von Borell et al., 2007) and was found in horses regularly receiving a relaxing massage (Kowalik et al., 2017). This increase in HF was not accompanied by an increase in RMSSD, although both represent vagal activity and are often correlated (Task Force of ESP and NASPE, 1996; Hagen et al., 2005; von Borell et al., 2007; Shaffer et al., 2014). However, changes in RMSSD were not consistently observed in other studies investigating different affective states in animals (Reefmann et al., 2012; Travain et al., 2016). RMSSD might therefore be a suboptimal indicator of animal affective states (Gygax et al., 2013; Tamioso et al., 2018). A different pattern emerged for SDNN: values increased from PRE to STIM in the “live” condition, and decreased again in POST, whereas in the “playback” condition, SDNN reached its highest values in POST. SDNN reflects influences of both parasympathetic and sympathetic activity (von Borell et al., 2007; Shaffer et al., 2014). Together with the decrease of RMSSD/SDNN during live talking, these findings might indicate that the “live” condition led to higher sympathetic activity during stroking and talking, possibly indicating positive arousal in response to being stroked (Tamioso et al., 2018). The increase of RMSSD/SDNN in “live” in POST is in line with increased values observed in sheep being brushed by a familiar human (Tamioso et al., 2018), and, in combination with the observed increase of HF in POST in “live,” indicates a shift toward vagal dominance after live talking. These patterns were not observed in the “playback” condition; contrarily, SDNN increased in POST, while RMSSD/SDNN and HF decreased slightly, possibly indicating a relative shift towards sympathetic regulation after stroking with “playback” stimulation.

In combination, the HRV results suggest that live talking may have been more pleasurable to the animals than “playback” and led to increased parasympathetic activity in the POST phase. They thus support the interpretation of a more pronounced relaxation effect indicated by the stronger decrease of HR in POST in “live” than in “playback.” The difference between the two auditory stimuli might be caused by losses of lower and higher frequencies of recorded sound, which have been found to cause a decline in dog's responses to commands, especially in the absence of certain non-verbal cues (Fukuzawa et al., 2005). As we could not measure the actual sound pressure reaching the animals' ears directly, we can neither exclude the possibility that there might have been other systematic differences between the acoustic signals produced by two sources, such as consistent differences in volume, which might have contributed to eliciting higher or lower arousal. Another difference between the situations might have been produced by a subconscious change of the stroker's body language or attention toward the animal during live talking. However, stroker behavior was standardized as far as possible – in both conditions, the stroker was calmly sitting next to the heifer's shoulder, focused on stroking the animal. Great care was taken to match the “playback” condition not only in body posture and calm breathing, but also in mental focus and intention of interacting gently with the animal, trying to minimize possible differences in non-verbal communication.

We hypothesized that the higher degree of standardization in the “playback” stimulus would lead to decreased variability in the data. However, the variability of the responses as indicated by the precision parameters revealed a conflicting pattern, indicating that the relationship between the degree of standardization of the treatment and the variability in the observed behavior is more complex than expected or has different effects on different parameters. The higher degree of standardization in “playback” stimuli did not lead to a generally reduced variability and therefore should not be the main criterion for preference of playback stimuli for gentle human-animal interactions in experimental settings.